Department of Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, UKDepartment of Developmental and Social Psychology (DPSS), University of Padova, Padova, Italy

Abstract

Language difficulties have been reported in children and adolescents who were born very preterm (< 32 weeks’ gestation) and associated with an atypical lateralisation of language processing, i.e. increased right-hemispheric engagement. This study used functional magnetic resonance imaging (fMRI) and spherical deconvolution tractography to study the hemodynamic responses associated with verbal fluency processing (easy and hard letter trials) and verbal fluency-related white matter fibre tracts in 64 very preterm born adults and 36 adult controls (mean age: 30 years). Tractography of the arcuate fasciculus (AF) and frontal aslant tract (FAT) was performed. Tracts were quantified in terms of mean volume, hindrance modulated orientational anisotropy, and lateralisation, assessed using a laterality index to indicate hemispheric dominance. During verbal fluency fMRI, very preterm participants displayed decreased hemodynamic response suppression in both the Easy > Rest and Hard > Rest conditions, compared to controls, in superior temporal gyrus, insula, thalamus and sensorimotor cortex, particularly in the right hemisphere. At the whole-group level, decreased hemodynamic response suppression in the right sensorimotor cortex was associated with worse on-line performance on the hard letter trials. Increased left-laterality in the AF was present alongside increased right hemispheric hemodynamic response suppression in controls. When only right-handed participants were considered, decreased hemodynamic response suppression in the right superior temporal gyrus during hard letter trials was related to weaker left and right FAT white matter integrity in the preterm group only. These results show that verbal fluency is affected by altered functional lateralisation in adults who were born very preterm.

Significance Statement This is the first study to use both functional and structural magnetic resonance imaging to assess the neuro-anatomy of verbal fluency in very preterm born adults. Less suppression of brain activation was observed in very preterm adults compared to controls in several brain regions during completion of both easy and hard verbal fluency trials. Furthermore, across all subjects, decreased brain activity suppression in the right sensorimotor cortex was associated with worse on-line performance on the hard letter trials. Increased left-laterality in the arcuate fasciculus, a language-related white matter tract, was present alongside increased right hemispheric brain activity suppression in controls. These findings suggest that alterations in the typical development of left-lateralisation in very preterm individuals are still present in adulthood.